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Article ; Online: Imaging methods in mechanosensing: a historical perspective and visions for the future.

Lavrenyuk, Kirill / Conway, Daniel / Dahl, Kris Noel

2021 Volume 32, Issue 9, Page(s) 842–854

Abstract: Over the past three decades, as mechanobiology has become a distinct area of study, researchers have developed novel imaging tools to discover the pathways of biomechanical signaling. Early work with substrate engineering and particle tracking ... ...

Abstract	Over the past three decades, as mechanobiology has become a distinct area of study, researchers have developed novel imaging tools to discover the pathways of biomechanical signaling. Early work with substrate engineering and particle tracking demonstrated the importance of cell-extracellular matrix interactions on the cell cycle as well as the mechanical flux of the intracellular environment. Most recently, tension sensor approaches allowed directly measuring tension in cell-cell and cell-substrate interactions. We retrospectively analyze how these various optical techniques progressed the field and suggest our vision forward for a unified theory of cell mechanics, mapping cellular mechanosensing, and novel biomedical applications for mechanobiology.
MeSH term(s)	Animals ; Biomechanical Phenomena/physiology ; Biophysics/methods ; Biophysics/trends ; Cell Differentiation ; Extracellular Matrix/metabolism ; Humans ; Mechanotransduction, Cellular/physiology ; Optical Imaging/methods ; Optical Imaging/trends ; Signal Transduction
Language	English
Publishing date	2021-03-31
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	1098979-1
ISSN	1939-4586 ; 1059-1524
ISSN (online)	1939-4586
ISSN	1059-1524
DOI	10.1091/mbc.E20-10-0671
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Article ; Online: A single stiffened nucleus alters cell dynamics and coherence in a monolayer.

Parreira, Maria Teresa / Lavrenyuk, Kirill / Sanches, João M / Dahl, Kris Noel

Cytoskeleton (Hoboken, N.J.)

2021 Volume 78, Issue 6, Page(s) 277–283

Abstract: Force transmission throughout a monolayer is the result of complex interactions between cells. Monolayer adaptation to force imbalances such as singular stiffened cells provides insight into the initiation of disease and fibrosis. Here, NRK-52E cells ... ...

Abstract	Force transmission throughout a monolayer is the result of complex interactions between cells. Monolayer adaptation to force imbalances such as singular stiffened cells provides insight into the initiation of disease and fibrosis. Here, NRK-52E cells transfected with ∆50LA, which significantly stiffens the nucleus. These stiffened cells were sparsely placed in a monolayer of normal NRK-52E cells. Through morphometric analysis and temporal tracking, the impact of the singular stiffened cells shows a pivotal role in mechanoresponse of the monolayer. A method for a detailed analysis of the spatial aspect and temporal progression of the nuclear boundary was developed and used to achieve a full description of the phenotype and dynamics of the monolayers under study. Our findings reveal that cells are highly sensitive to the presence of mechanically impaired neighbors, leading to generalized loss of coordination in collective cell migration, but without seemingly affecting the potential for nuclear lamina fluctuations of neighboring cells. Reduced translocation in neighboring cells appears to be compensated by an increase in nuclear rotation and dynamic variation of shape, suggesting a "frustration" of cells and maintenance of motor activity. Interestingly, some characteristics of the behavior of these cells appear to be dependent on the distance to a ∆50LA cell, pointing to compensatory behavior in response to force transmission imbalances in a monolayer. These insights may suggest the long-range impacts of single cell defects related to tissue dysfunction.
MeSH term(s)	Cell Movement ; Epithelial Cells ; Fibrosis ; Humans
Language	English
Publishing date	2021-04-22
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2534372-5
ISSN	1949-3592 ; 1949-3584
ISSN (online)	1949-3592
ISSN	1949-3584
DOI	10.1002/cm.21660
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Article ; Online: Correction: Spatially Resolved Quantification of Chromatin Condensation through Differential Local Rheology in Cell Nuclei Fluorescence Lifetime Imaging.

Spagnol, Stephen T / Dahl, Kris Noel

PloS one

2016 Volume 11, Issue 4, Page(s) e0154639

Abstract: This corrects the article DOI: 10.1371/journal.pone.0146244.]. ...

Abstract	[This corrects the article DOI: 10.1371/journal.pone.0146244.].
Language	English
Publishing date	2016
Publishing country	United States
Document type	Published Erratum
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0154639
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Article: CRISPR Cas13-Based Tools to Track and Manipulate Endogenous Telomeric Repeat-Containing RNAs in Live Cells.

Xu, Meng / Chigumira, Tafadzwa / Chen, Ziheng / Tones, Jason / Zhao, Rongwei / Dahl, Kris Noel / Chenoweth, David M / Zhang, Huaiying

Frontiers in molecular biosciences

2022 Volume 8, Page(s) 785160

Abstract: TERRA, TElomeric Repeat-containing RNA, is a long non-coding RNA transcribed from telomeres. Emerging evidence indicates that TERRA regulates telomere maintenance and chromosome end protection in normal and cancerous cells. However, the mechanism of how ... ...

Abstract	TERRA, TElomeric Repeat-containing RNA, is a long non-coding RNA transcribed from telomeres. Emerging evidence indicates that TERRA regulates telomere maintenance and chromosome end protection in normal and cancerous cells. However, the mechanism of how TERRA contributes to telomere functions is still unclear, partially owing to the shortage of approaches to track and manipulate endogenous TERRA molecules in live cells. Here, we developed a method to visualize TERRA in live cells via a combination of CRISPR Cas13 RNA labeling and SunTag technology. Single-particle tracking reveals that TERRA foci undergo anomalous diffusion in a manner that depends on the timescale and telomeric localization. Furthermore, we used a chemically-induced protein dimerization system to manipulate TERRA subcellular localization in live cells. Overall, our approaches to monitor and control TERRA locations in live cells provide powerful tools to better understand its roles in telomere maintenance and genomic integrity.
Language	English
Publishing date	2022-01-31
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2814330-9
ISSN	2296-889X
ISSN	2296-889X
DOI	10.3389/fmolb.2021.785160
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Article ; Online: The Elephant in the Cell: Nuclear Mechanics and Mechanobiology.

Jones, Michelle L / Dahl, Kris Noel / Lele, Tanmay P / Conway, Daniel E / Shenoy, Vivek / Ghosh, Soham / Szczesny, Spencer E

Journal of biomechanical engineering

2022 Volume 144, Issue 8

Abstract: The 2021 Summer Biomechanics, Bioengineering, and Biotransport Conference (SB3C) featured a workshop titled "The Elephant in the Room: Nuclear Mechanics and Mechanobiology." The goal of this workshop was to provide a perspective from experts in the field ...

Abstract	The 2021 Summer Biomechanics, Bioengineering, and Biotransport Conference (SB3C) featured a workshop titled "The Elephant in the Room: Nuclear Mechanics and Mechanobiology." The goal of this workshop was to provide a perspective from experts in the field on the current understanding of nuclear mechanics and its role in mechanobiology. This paper reviews the major themes and questions discussed during the workshop, including historical context on the initial methods of measuring the mechanical properties of the nucleus and classifying the primary structures dictating nuclear mechanics, physical plasticity of the nucleus, the emerging role of the linker of nucleoskeleton and cytoskeleton (LINC) complex in coupling the nucleus to the cytoplasm and driving the behavior of individual cells and multicellular assemblies, and the computational models currently in use to investigate the mechanisms of gene expression and cell signaling. Ongoing questions and controversies, along with promising future directions, are also discussed.
MeSH term(s)	Biophysics ; Cell Nucleus ; Cytoskeleton/metabolism ; Microtubules/metabolism ; Nuclear Matrix/metabolism
Language	English
Publishing date	2022-02-07
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	243094-0
ISSN	1528-8951 ; 0148-0731
ISSN (online)	1528-8951
ISSN	0148-0731
DOI	10.1115/1.4053797
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Article ; Online: Chromatin condensation regulates endothelial cell adaptation to shear stress.

Danielsson, Brooke E / Tieu, Katie V / Spagnol, Stephen T / Vu, Kira K / Cabe, Jolene I / Raisch, Tristan B / Dahl, Kris Noel / Conway, Daniel E

Molecular biology of the cell

2022 Volume 33, Issue 11, Page(s) ar101

Abstract: Vascular endothelial cells (ECs) have been shown to be mechanoresponsive to the forces of blood flow, including fluid shear stress (FSS), the frictional force of blood on the vessel wall. Recent reports have shown that FSS induces epigenetic changes in ... ...

Abstract	Vascular endothelial cells (ECs) have been shown to be mechanoresponsive to the forces of blood flow, including fluid shear stress (FSS), the frictional force of blood on the vessel wall. Recent reports have shown that FSS induces epigenetic changes in chromatin. Epigenetic changes, such as methylation and acetylation of histones, not only affect gene expression but also affect chromatin condensation, which can alter nuclear stiffness. Thus, we hypothesized that changes in chromatin condensation may be an important component for how ECs adapt to FSS. Using both in vitro and in vivo models of EC adaptation to FSS, we observed an increase in histone acetylation and a decrease in histone methylation in ECs adapted to flow as compared with static. Using small molecule drugs, as well as vascular endothelial growth factor, to change chromatin condensation, we show that decreasing chromatin condensation enables cells to more quickly align to FSS, whereas increasing chromatin condensation inhibited alignment. Additionally, we show data that changes in chromatin condensation can also prevent or increase DNA damage, as measured by phosphorylation of γH2AX. Taken together, these results indicate that chromatin condensation, and potentially by extension nuclear stiffness, is an important aspect of EC adaptation to FSS.
MeSH term(s)	Acetylation ; Chromatin/metabolism ; Endothelial Cells/metabolism ; Histones/metabolism ; Stress, Mechanical ; Vascular Endothelial Growth Factor A
Chemical Substances	Chromatin ; Histones ; Vascular Endothelial Growth Factor A
Language	English
Publishing date	2022-07-27
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1098979-1
ISSN	1939-4586 ; 1059-1524
ISSN (online)	1939-4586
ISSN	1059-1524
DOI	10.1091/mbc.E22-02-0064
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Article ; Online: CRISPR Cas13-Based Tools to Track and Manipulate Endogenous Telomeric Repeat-Containing RNAs in Live Cells

Meng Xu / Tafadzwa Chigumira / Ziheng Chen / Jason Tones / Rongwei Zhao / Kris Noel Dahl / David M. Chenoweth / Huaiying Zhang

Frontiers in Molecular Biosciences, Vol

2022 Volume 8

Abstract	TERRA, TElomeric Repeat-containing RNA, is a long non-coding RNA transcribed from telomeres. Emerging evidence indicates that TERRA regulates telomere maintenance and chromosome end protection in normal and cancerous cells. However, the mechanism of how TERRA contributes to telomere functions is still unclear, partially owing to the shortage of approaches to track and manipulate endogenous TERRA molecules in live cells. Here, we developed a method to visualize TERRA in live cells via a combination of CRISPR Cas13 RNA labeling and SunTag technology. Single-particle tracking reveals that TERRA foci undergo anomalous diffusion in a manner that depends on the timescale and telomeric localization. Furthermore, we used a chemically-induced protein dimerization system to manipulate TERRA subcellular localization in live cells. Overall, our approaches to monitor and control TERRA locations in live cells provide powerful tools to better understand its roles in telomere maintenance and genomic integrity.
Keywords	RNA imaging ; TERRA ; lncRNA ; telomere ; CRISPR Cas13 ; chemical dimerizer ; Biology (General) ; QH301-705.5
Language	English
Publishing date	2022-01-01T00:00:00Z
Publisher	Frontiers Media S.A.
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Spatially Resolved Quantification of Chromatin Condensation through Differential Local Rheology in Cell Nuclei Fluorescence Lifetime Imaging.

Spagnol, Stephen T / Dahl, Kris Noel

PloS one

2016 Volume 11, Issue 1, Page(s) e0146244

Abstract: The linear sequence of DNA encodes access to the complete set of proteins that carry out cellular functions. Yet, much of the functionality appropriate for each cell is nested within layers of dynamic regulation and organization, including a hierarchy of ...

Abstract	The linear sequence of DNA encodes access to the complete set of proteins that carry out cellular functions. Yet, much of the functionality appropriate for each cell is nested within layers of dynamic regulation and organization, including a hierarchy of chromatin structural states and spatial arrangement within the nucleus. There remain limitations in our understanding of gene expression within the context of nuclear organization from an inability to characterize hierarchical chromatin organization in situ. Here we demonstrate the use of fluorescence lifetime imaging microscopy (FLIM) to quantify and spatially resolve chromatin condensation state using cell-permeable, DNA-binding dyes (Hoechst 33342 and PicoGreen). Through in vitro and in situ experiments we demonstrate the sensitivity of fluorescence lifetime to condensation state through the mechanical effects that accompany the structural changes and are reflected through altered viscosity. The establishment of FLIM for resolving and quantifying chromatin condensation state opens the door for single-measurement mechanical studies of the nucleus and for characterizing the role of genome structure and organization in nuclear processes that accompany physiological and pathological changes.
MeSH term(s)	Bacteriophage lambda/genetics ; Cell Nucleus ; Chromatin ; DNA, Viral ; Fluorescent Dyes ; Heterochromatin ; Human Umbilical Vein Endothelial Cells ; Humans ; Microscopy, Fluorescence ; Optical Imaging/methods ; Rheology/methods
Chemical Substances	Chromatin ; DNA, Viral ; Fluorescent Dyes ; Heterochromatin
Language	English
Publishing date	2016-01-14
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0146244
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Correction

Stephen T Spagnol / Kris Noel Dahl

PLoS ONE, Vol 11, Iss 4, p e

Spatially Resolved Quantification of Chromatin Condensation through Differential Local Rheology in Cell Nuclei Fluorescence Lifetime Imaging.

2016 Volume 0154639

Abstract: This corrects the article DOI:10.1371/journal.pone.0146244.]. ...

Abstract	[This corrects the article DOI:10.1371/journal.pone.0146244.].
Keywords	Medicine ; R ; Science ; Q
Language	English
Publishing date	2016-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Active cytoskeletal force and chromatin condensation independently modulate intranuclear network fluctuations.

Spagnol, Stephen T / Dahl, Kris Noel

Integrative biology : quantitative biosciences from nano to macro

2014 Volume 6, Issue 5, Page(s) 523–531

Abstract: Chromatin remodeling, including the movement of genes and regulatory factors, precedes or accompanies stimulated changes in gene expression. Here we quantify chromatin fluctuations in primary human cells using particle-tracking microrheology and ... ...

Abstract	Chromatin remodeling, including the movement of genes and regulatory factors, precedes or accompanies stimulated changes in gene expression. Here we quantify chromatin fluctuations in primary human cells using particle-tracking microrheology and determine the physical mechanisms which influence chromatin reorganization. We find that intranuclear movements are enhanced beyond thermal motion by active force generation from cytoskeletal motor activity propagated through the LINC complex; intranuclear movements are also dependent on the viscoelasticity of the DNA-protein polymer network. Chromatin movements were dramatically altered by modulation of chromatin condensation state, which we independently verified using fluorescence lifetime imaging microscopy (FLIM). These findings suggest that chromatin condensation and cytoskeletal force generation play distinct functional roles in regulating intranuclear movements, and these effects are decoupled as measured by particle tracking. We further utilize this approach in identifying the nuclear responsiveness of primary human endothelial cells to vascular endothelial growth factor (VEGF): early in the response chromatin movements increase and are dominated by cytoskeletal force, which transitions at later times to a chromatin decondensation event. Given the hierarchical genome organization in primary cells, our work generally suggests an important role for force generation and chromatin mechanics in altered gene expression kinetics.
MeSH term(s)	Cell Nucleus/physiology ; Chi-Square Distribution ; Chromatin Assembly and Disassembly/physiology ; Cytoskeleton/physiology ; Human Umbilical Vein Endothelial Cells/physiology ; Humans ; Microscopy, Fluorescence ; Rheology ; Vascular Endothelial Growth Factor A/physiology
Chemical Substances	Vascular Endothelial Growth Factor A
Language	English
Publishing date	2014-05
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2480063-6
ISSN	1757-9708 ; 1757-9694
ISSN (online)	1757-9708
ISSN	1757-9694
DOI	10.1039/c3ib40226f
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